Neural mechanisms of emotion during shifting perspectives and recognizing new information: An fMRI study

Kazutaka Ueda; Xiaoxiang Wu; Hideyoshi Yanagisawa

doi:10.1371/journal.pone.0309273

Peer Review History

Original SubmissionAugust 8, 2024
8 Aug 2024 Author Response https://doi.org/10.1371/journal.pone.0309273.r001
Decision Letter - Wi Hoon Jung, Editor PONE-D-24-33040Neural mechanisms of emotion during shifting perspectives and recognizing new information: An fMRI studyPLOS ONE Dear Dr. Yanagisawa, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Apr 26 2025 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org . When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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Currently, your Funding Statement reads as follows: “Initials of author who received the grant: Hideyoshi Yanagisawa (H.Y) Grant number: 21H03528 Full name of funder: Japan Society for the Promotion of Science URL of the funder website: https://www.jsps.go.jp/english/e-grants/ ” Please include your amended statements within your cover letter; we will change the online submission form on your behalf. 3. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. Additional Editor Comments (if provided): Please review the comments made by the reviewer below regarding this study and revise the manuscript. In particular, we ask that you revise the conclusions and interpretations of the results of this study. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: The paper "Neural mechanisms of emotion during shifting perspectives and recognizing new information: An fMRI study" applies the free energy principle and utilizes fMRI to investigate a mathematical model's ability to predict emotions when individuals shift perspectives to acknowledge alternative information about an event. The study concludes that interest relates to unexpected yet easily comprehensible new concepts. The fMRI study demonstrates a well-structured database design, and the conclusions are statistically supported. However, some issues require revision. Once these concerns are addressed, I recommend the manuscript for publication. The authors assert (lines 352-354) that "the amygdala [21–25] and hippocampus, which showed increased connectivity in the high-difficulty condition, are related to positive emotion, and these results are consistent with the model predictions." However, literature does not support this conclusion. While the amygdala can respond to positive stimuli, it is preferentially activates in fearful conditions. Therefore, a more accurate conclusion would be a generalized response to emotionally valenced stimuli. The authors need to justify their conclusion (lines 349-350) as to why shifting from recognition based on certain beliefs to recognition based on uncertain beliefs results in a smaller recognition distance and easier recognition. In reality, the expected response is a smaller recognition distance for recognition based on certain beliefs. Creativity is not uniformly distributed among individuals in society. Therefore, providing information on the study subjects' backgrounds (such as their familiarity with card tricks or their occupations in creative fields) could enhance the applicability and conclusions of the results. While the data presented support the hypothesis, the relationship is not straightforward. Exploring alternative explanations for the results would create a stronger argument. ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean? ). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy . 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Revision 1
23 May 2025 Author Response Manuscript ID: PONE-D-24-33040 Title: Neural mechanisms of emotion during shifting perspectives and recognizing new information: An fMRI study Dear Editor, We are most grateful to you and the reviewers for the helpful comments on the original version of our manuscript. In response to the reviewers' comments, we have revised the manuscript. We hope that the revised version of our paper is now suitable for publication in PLOS One and we look forward to hearing from you at your earliest convenience. Sincerely, Hideyoshi Yanagisawa, Ph.D. Our responses to the Editor and reviewers have been uploaded respectively. Reviewer #1 Comments and Responses We are grateful to reviewer #1 for the critical comments and useful suggestions that have helped us to improve our paper considerably. As indicated in the responses that follow, we have taken the comments and suggestions into account in the revised version of our paper. Reviewer #1’s Comment 1 The authors assert (lines 352-354) that "the amygdala [21–25] and hippocampus, which showed increased connectivity in the high-difficulty condition, are related to positive emotion, and these results are consistent with the model predictions." However, literature does not support this conclusion. While the amygdala can respond to positive stimuli, it is preferentially activates in fearful conditions. Therefore, a more accurate conclusion would be a generalized response to emotionally valenced stimuli. Response 1 We sincerely thank the reviewer for identifying this important issue. Upon reviewing our manuscript, we found that the experimental result itself was correctly analyzed and presented in the figures and results section, but the description in the Discussion (original manuscript, lines 352–354) mistakenly stated that the increased connectivity between the amygdala and hippocampus occurred in the high-difficulty condition. In fact, as correctly shown in Figure 8b and described in the results section, this increased connectivity was observed in the low-difficulty condition, in which participants were able to more easily reinterpret the card trick from a different perspective. We have now corrected the text in the Discussion to accurately reflect this. Furthermore, we appreciate the reviewer’s clarification regarding the role of the amygdala in emotion processing. We have revised the interpretation to avoid implying a specific emotional valence, as the amygdala is known to respond to both positive and negative emotional stimuli. The revised wording more accurately reflects the scope of the empirical findings and their relationship to our theoretical model, emphasizing emotional salience and cognitive engagement rather than valence-specific emotion. We revised the sentence in the Discussion section (lines 353–359) to read: “Additionally, in the low-difficulty condition, increased functional connectivity between the amygdala [21–25] and hippocampus was observed. The amygdala is involved in processing emotionally salient stimuli, regardless of valence. This result may reflect heightened emotional salience during successful perspective shifts. This interpretation aligns with the model’s assumption that when perspective is shifted from a certain belief to a more uncertain belief, and the recognition distance is relatively small, greater disfluency reduction and emotional engagement are more likely to occur.” Reviewer #1’s Comment 2 The authors need to justify their conclusion (lines 349-350) as to why shifting from recognition based on certain beliefs to recognition based on uncertain beliefs results in a smaller recognition distance and easier recognition. In reality, the expected response is a smaller recognition distance for recognition based on certain beliefs. Response 2 Thank you for raising this important point. We agree that the original wording in lines 349–350 in original manuscript may have inadvertently suggested a direct causal relationship—that shifting from certain to uncertain beliefs inherently leads to smaller recognition distances and easier recognition. In fact, our model assumes a more nuanced prediction: when a recognition shift occurs from a certain to an uncertain belief, and the recognition distance is small, then disfluency reduction is greater, leading to more cognitively fluent recognition and increased emotional engagement. We also wish to clarify that this prediction was explicitly stated in the Introduction of the original manuscript. On lines 134–137, we wrote: “Specifically, by measuring human brain functions, we tested the prediction that a smaller recognition distance (i.e., easier recognition) would produce more positive emotions, such as interest, when shifting from recognition based on certain beliefs to recognition based on uncertain beliefs.” To improve clarity and more accurately reflect the theoretical framework, we have revised the Discussion section (lines 346–353) to the following: “These results suggest that when recognition shifts from a certain belief to a more uncertain one, greater activity in the cingulate gyrus [18–20] and hippocampus [26] is observed, particularly in cases in which the recognition distance is relatively small and recognition becomes easier. Given that both regions have been previously associated with the processing of positive emotional experiences, this neural pattern supports our model’s prediction that recognition distance, rather than belief uncertainty alone, is a key determinant of disfluency reduction and emotionally engaging responses.” This revision eliminates the oversimplified causality in the original sentence and more accurately conveys the model’s condition-dependent prediction. Reviewer #1’s Comment 3 Creativity is not uniformly distributed among individuals in society. Therefore, providing information on the study subjects' backgrounds (such as their familiarity with card tricks or their occupations in creative fields) could enhance the applicability and conclusions of the results. Response 3 Thank you for this valuable suggestion. As described in the Participants section of the Methods, all participants were individuals who had not mastered card magic skills and thus had no specialized expertise in the specific domain of the task. However, we did not assess the participants’ broader creative profiles, including their occupations in creative fields or general familiarity with visual illusions or perspective-shifting tasks. We have now acknowledged this as a limitation in the Discussion section (lines 371-376): “A limitation of this experiment is that we did not collect information about participants’ prior experience with magic tricks, their occupations in creative fields, or their general creative background. Although all participants had not mastered card magic skills, individual differences in creative training, profession, or familiarity with similar illusions could influence the ease of recognition or emotional responses. Future studies should consider assessing such background factors to better account for variance in emotional and cognitive responses.” Reviewer #1’s Comment 4 While the data presented support the hypothesis, the relationship is not straightforward. Exploring alternative explanations for the results would create a stronger argument. Response 4 Thank you for this thoughtful and constructive comment. We agree that the relationship between the observed brain activity and our model’s predictions may not be entirely straightforward and that alternative explanations merit consideration. In the revised manuscript, we have added a paragraph in the Discussion (lines 360-370) acknowledging this and outlining several alternative interpretations. “Although our interpretation emphasizes that increased activation and connectivity in regions such as the anterior cingulate cortex, hippocampus, and amygdala may reflect disfluency reduction and emotional engagement during successful perspective shifts, we acknowledge that other interpretations are also plausible. For example, anterior cingulate cortex activity may reflect general cognitive control or conflict monitoring [28] in response to updating beliefs. Hippocampal activity may reflect indicate episodic memory retrieval [27] or novelty processing [29]. Similarly, increased connectivity between the amygdala and hippocampus in the low-difficulty condition may reflect enhanced attentional allocation to emotionally meaningful content [30]. These possibilities suggest that the observed neural responses may involve a combination of emotional, mnemonic, and attentional mechanisms. Future studies could incorporate more targeted designs to disentangle these processes.” References 18. Lane RD, Fink GR, Chau PM-L, Dolan RJ. Neural activation during selective attention to subjective emotional responses. NeuroReport. 1997;8: 3969–3972. doi: 10.1097/00001756-199712220-00024, Pubmed:9462476. 19. Matsunaga M, Kawamichi H, Koike T, Yoshihara K, Yoshida Y, Takahashi HK, et al. Structural and functional associations of the rostral anterior cingulate cortex with subjective happiness. Neuroimage. 2016;134: 132–141. doi: 10.1016/j.neuroimage.2016.04.020, Pubmed:27085503. 20. Scharnowski F, Nicholson AA, Pichon S, Rosa MJ, Rey G, Eickhoff SB, et al. The role of the subgenual anterior cingulate cortex in dorsomedial prefrontal–amygdala neural circuitry during positive‐social emotion regulation. Hum Brain Mapp. 2020;41: 3100–3118. doi: 10.1002/hbm.25001, Pubmed:32309893. 21. Baxter MG, Murray EA. The amygdala and reward. Nat Rev Neurosci. 2002;3: 563–573. doi: 10.1038/nrn875, Pubmed:12094212. 22. Bonnet L, Comte A, Tatu L, Millot JL, Moulin T, Medeiros de Bustos E. The role of the amygdala in the perception of positive emotions: an “intensity detector”. Front Behav Neurosci. 2015;9: 178. doi: 10.3389/fnbeh.2015.00178, Pubmed:26217205. 23. Canli T, Sivers H, Whitfield SL, Gotlib IH, Gabrieli JDE. Amygdala response to happy faces as a function of extraversion. Science. 2002;296: 2191. doi: 10.1126/science.1068749, Pubmed:12077407. 24. Koepp MJ, Hammers A, Lawrence AD, Asselin MC, Grasby PM, Bench CJ. Evidence for endogenous opioid release in the amygdala during positive emotion. Neuroimage. 2009;44: 252–256. doi: 10.1016/j.neuroimage.2008.08.032, Pubmed:18809501. 25. Murray EA. The amygdala, reward and emotion. Trends Cogn Sci. 2007;11: 489–497. doi: 10.1016/j.tics.2007.08.013, Pubmed:17988930. 26. Gruber MJ, Gelman BD, Ranganath C. States of curiosity modulate hippocampus-dependent learning via the dopaminergic circuit. Neuron. 2014;84: 486–496. doi: 10.1016/j.neuron.2014.08.060, Pubmed:25284006. 28. Kerns JG, Cohen JD, MacDonald III AW, Cho RY, Stenger VA, Carter CS. Anterior cingulate conflict monitoring and adjustments in control. Science. 2004;303: 1023–1026. doi: 10.1126/science.1089910 29. Duncan K, Ketz N, Inati SJ, Davachi L. Evidence for area CA1 as a match/mismatch detector: A high‐resolution fMRI study of the human hippocampus. Hippocampus. 2012;22: 389–398. doi: 10.1002/hipo.20933 30. Zheng J, Anderson KL, Leal SL, Shestyuk A, Gulsen G, Mnatsakanyan L, Vadera S, Hsu FPK, Yassa MA, Knight RT. Lin JJ. Amygdala-hippocampal dynamics during salient information processing. Nat Commun. 2017;8: 14413. doi: 10.1038/ncomms14413 Attachments Attachment Submitted filename: Response_to_Reviewers.docx https://doi.org/10.1371/journal.pone.0309273.r003
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Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes ****** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: Thank you for your thoughtful responses to my comments on the manuscript. The revisions effectively address the concerns I raised, and they have significantly strengthened the manuscript. With these improvements, I am pleased to recommend the manuscript for publication. ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean? ). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy . Reviewer #1: Yes: Eva K Deli ******** Attachments Attachment Submitted filename: reviewer response.docx https://doi.org/10.1371/journal.pone.0309273.r004
Formally Accepted
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